Darin Morgan was named by his parents after pop vocalist Bobby Darin and grew up in Syracuse, New York, during which time his tastes tended towards vintage comedy film, especially the work of classic slapstick performers like Charlie Chaplin, Buster Keaton, and Harold Lloyd. Darin followed his brother, Glen, into the film program at Loyola Marymount University, where he made a six-minute mockumentary called "Legends of Doo-Wop" that allegedly revealed the untold story of two 1960s pop producers who supposedly were secretly responsible for sound effects that had made "Everyday" and "Stand By Me" become hits. The short film became a sensation on campus and, in an incredible turn, it won Darin Morgan a three-film deal with Tri-Star at the relatively young age of nineteen. Morgan, however, soon found himself miserable and out of work. He also dropped out of Loyola Marymount University before completing his studies.

He was subsequently cast in a few acting roles, including a part in an episode of The Commish, and it was in 1994 that his association with The X-Files began when he starred in "The Host", his brother having already been assigned to write for the series with writing partner James Wong. The writing duo had written several fan favorites in the series' first season, including "Beyond the Sea", Darin Morgan's favorite episode of The X-Files that, fittingly, was named after one of Bobby Darin's most famous songs.

Darin Morgan subsequently received a story credit for "Blood", the next episode to be produced following "The Host", after his brother, Glen, enlisted Darin's help with fleshing out the story while Glen was writing the episode with James Wong. As a result of his assistance on the episode, Darin was offered a job on the show's writing staff, alongside his brother. Despite his agent's pleas to the contrary, Darin almost turned down the job, considering himself first and foremost a comedy writer. Although he was also worried that his sensibilities would clash with the dark palette of The X-Files, Darin reluctantly accepted the job and, even though he ultimately wrote only four episodes for the series, he brought a comedic flair to The X-Files that had not previously existed on the series but influenced other members of the writing staff to occasionally mimic his inspirational writing style.

Following the first of these four episodes, "Humbug", Darin Morgan also served as story editor throughout the duration of the series' third season, returning the next season to play his final part in the series as Eddie Van Blundt. He continued to serve as consulting producer through Millennium's second season, bringing his comedic style to two episodes in that season that he also directed, including one that was a sequel to the last episode he had written for The X-Files, both episodes featuring writer José Chung, the first character to cross-over between the two series.